The on‐again, off‐again relationship between mitochondrial genomes and species boundaries

Abstract

The study of reproductive isolation and species barriers frequently focuses on mitochondrial genomes and has produced two alternative and almost diametrically opposed narratives. On one hand, mtDNA may be at the forefront of speciation events, with co-evolved mitonuclear interactions responsible for some of the earliest genetic incompatibilities arising among isolated populations. On the other hand, there are numerous cases of introgression of mtDNA across species boundaries even when nuclear gene flow is restricted. We argue that these seemingly contradictory patterns can result from a single underlying cause. Specifically, the accumulation of deleterious mutations in mtDNA creates a problem with two alternative evolutionary solutions. In some cases, compensatory or epistatic changes in the nuclear genome may ameliorate the effects of mitochondrial mutations, thereby establishing coadapted mitonuclear genotypes within populations and forming the basis of reproductive incompatibilities between populations. Alternatively, populations with high mitochondrial mutation loads may be rescued by replacement with a more fit, foreign mitochondrial haplotype. Coupled with many nonadaptive mechanisms of introgression that can preferentially affect cytoplasmic genomes, this form of adaptive introgression may contribute to the widespread discordance between mitochondrial and nuclear genealogies. Here, we review recent advances related to mitochondrial introgression and mitonuclear incompatibilities, including the potential for cointrogression of mtDNA and interacting nuclear genes. We also address an emerging controversy over the classic assumption that selection on mitochondrial genomes is inefficient and discuss the mechanisms that lead lineages down alternative evolutionary paths in response to mitochondrial mutation accumulation.

Modern human origins: multiregional evolution of autosomes and East Asia origin of Y and mtDNA

“…Sharing of physiology should be informative for a phonetic approach of phylogeny. Coevolution of mtDNA, Y, and autosomes has been found by many previous studies (25,(65)(66)(67)(68), which may play a key role in the diversification into multiple haplotypes during AMH radiation from its place of origin to other regions by hybridization with archaic humans. People who have stayed relatively unchanged in physiology and living environments from the ancestor would be expected to have few deviations from the ancestor haplotype and their present day living place would indicate place of origin for the ancestor.…”

“…Most SNPs in these DNAs can be proven to be under selection, e.g. certain SNPs or haplotypes of mtDNA or Y chr are known to be related to human diseases or compatibility with nuclear genomes (25,(61)(62)(63)(64)(65). Sharing of alleles of mtDNA or Y chr should mean similar selection, reflecting both environments and physiology or primarily physiology when saturation has been reached.…”

Divergent mitochondrial lineages arose within a large, panmictic population of the Savannah sparrow (Passerculus sandwichensis)

“…This runs counter to theoretical and empirical inferences that have shown asymmetric introgression tends to occur in the direction from larger to smaller populations (e.g., Currat et al, ; Sarver et al, ). Alternatively, selection for the northwestern Mexico mtDNA haplotypes could result in its introgression and sweep through the nominate population (e.g., Sloan et al, ). In this case, we would expect the favoured mtDNA haplotype to either completely displace the less advantageous haplotype or displace it in parts of the species range where it is favourable.…”

Testing an hypothesis of hybrid zone movement for toads in France

“…Concordant and narrow clines (steep at the centre and with distinct tails) suggest that the hybrid zone is maintained by a balance between strong selection and dispersal, as opposed to displaced and wide clines indicating that selection against hybrids is low (shallow slope without distinct tails; Barton & Gale, ). Displaced and discordant clines exist in many species, both for nuclear and mitochondrial markers, and may be caused by sex‐biased gene flow or by adaptive introgression (Bonnet, Leblois, Rousset, & Crochet, ; Excoffier, Foll, & Petit, ; Mallet, ; Sloan, Havird, & Sharbrough, ; Toews & Brelsford, ; While et al, ). However, displaced and discordant clines may also be caused by hybrid zone movement, when a trail of genetic material from the overtaken species remains present in the overtaking species (Arntzen, de Vries, Canestrelli, & Martínez‐Solano, ; Excoffier et al, ; Gay, Crochet, Bell, & Lenormand, ; Rohwer, Bermingham, & Wood, ; Wielstra, Burke, Butlin, Avcı et al, ).…”